Holobiont chronobiology: mycorrhiza may be a key to linking aboveground and underground rhythms.

Abstract

Circadian clocks are nearly ubiquitous timing mechanisms that can orchestrate rhythmic behavior and gene expression in a wide range of organisms. Clock mechanisms are becoming well understood in fungal, animal, and plant model systems, yet many of these organisms are surrounded by a complex and diverse microbiota which should be taken into account when examining their biology. Of particular interest are the symbiotic relationships between organisms that have coevolved over time, forming a unit called a holobiont. Several studies have now shown linkages between the circadian rhythms of symbiotic partners. Interrelated regulation of holobiont circadian rhythms seems thus important to coordinate shifts in activity over the day for all the partners. Therefore, we suggest that the classical view of "chronobiological individuals" should include "a holobiont" rather than an organism. Unfortunately, mechanisms that may regulate interspecies temporal acclimation and the evolution of the circadian clock in holobionts are far from being understood. For the plant holobiont, our understanding is particularly limited. In this case, the holobiont encompasses two different ecosystems, one above and the other below the ground, with the two potentially receiving timing information from different synchronizing signals (Zeitgebers). The arbuscular mycorrhizal (AM) symbiosis, formed by plant roots and fungi, is one of the oldest and most widespread associations between organisms. By mediating the nutritional flux between the plant and the many microbes in the soil, AM symbiosis constitutes the backbone of the plant holobiont. Even though the importance of the AM symbiosis has been well recognized in agricultural and environmental sciences, its circadian chronobiology remains almost completely unknown. We have begun to study the circadian clock of arbuscular mycorrhizal fungi, and we compile and here discuss the available information on the subject. We propose that analyzing the interrelated temporal organization of the AM symbiosis and determining its underlying mechanisms will advance our understanding of the role and coordination of circadian clocks in holobionts in general.